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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Structural insights into coronavirus entry</title>
<author><name sortKey="Tortorici, M Alejandra" sort="Tortorici, M Alejandra" uniqKey="Tortorici M" first="M. Alejandra" last="Tortorici">M. Alejandra Tortorici</name>
<affiliation><nlm:aff id="af0010">Department of Biochemistry, University of Washington, Seattle, WA, United States</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af0015">Institut Pasteur, Unité de Virologie Structurale, Paris, France</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af0020">CNRS UMR 3569, Unité de Virologie Structurale, Paris, France</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Veesler, David" sort="Veesler, David" uniqKey="Veesler D" first="David" last="Veesler">David Veesler</name>
<affiliation><nlm:aff id="af0010">Department of Biochemistry, University of Washington, Seattle, WA, United States</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">31522710</idno>
<idno type="pmc">7112261</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7112261</idno>
<idno type="RBID">PMC:7112261</idno>
<idno type="doi">10.1016/bs.aivir.2019.08.002</idno>
<date when="2019">2019</date>
<idno type="wicri:Area/Pmc/Corpus">000909</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000909</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Structural insights into coronavirus entry</title>
<author><name sortKey="Tortorici, M Alejandra" sort="Tortorici, M Alejandra" uniqKey="Tortorici M" first="M. Alejandra" last="Tortorici">M. Alejandra Tortorici</name>
<affiliation><nlm:aff id="af0010">Department of Biochemistry, University of Washington, Seattle, WA, United States</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af0015">Institut Pasteur, Unité de Virologie Structurale, Paris, France</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af0020">CNRS UMR 3569, Unité de Virologie Structurale, Paris, France</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Veesler, David" sort="Veesler, David" uniqKey="Veesler D" first="David" last="Veesler">David Veesler</name>
<affiliation><nlm:aff id="af0010">Department of Biochemistry, University of Washington, Seattle, WA, United States</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Advances in Virus Research</title>
<idno type="ISSN">0065-3527</idno>
<idno type="eISSN">1557-8399</idno>
<imprint><date when="2019">2019</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Coronaviruses (CoVs) have caused outbreaks of deadly pneumonia in humans since the beginning of the 21st century. The severe acute respiratory syndrome coronavirus (SARS-CoV) emerged in 2002 and was responsible for an epidemic that spread to five continents with a fatality rate of 10% before being contained in 2003 (with additional cases reported in 2004). The Middle-East respiratory syndrome coronavirus (MERS-CoV) emerged in the Arabian Peninsula in 2012 and has caused recurrent outbreaks in humans with a fatality rate of 35%. SARS-CoV and MERS-CoV are zoonotic viruses that crossed the species barrier using bats/palm civets and dromedary camels, respectively. No specific treatments or vaccines have been approved against any of the six human coronaviruses, highlighting the need to investigate the principles governing viral entry and cross-species transmission as well as to prepare for zoonotic outbreaks which are likely to occur due to the large reservoir of CoVs found in mammals and birds. Here, we review our understanding of the infection mechanism used by coronaviruses derived from recent structural and biochemical studies.</p>
</div>
</front>
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<pmc article-type="other"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Adv Virus Res</journal-id>
<journal-id journal-id-type="iso-abbrev">Adv. Virus Res</journal-id>
<journal-title-group><journal-title>Advances in Virus Research</journal-title>
</journal-title-group>
<issn pub-type="ppub">0065-3527</issn>
<issn pub-type="epub">1557-8399</issn>
<publisher><publisher-name>Elsevier Inc.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31522710</article-id>
<article-id pub-id-type="pmc">7112261</article-id>
<article-id pub-id-type="publisher-id">S0065-3527(19)30028-4</article-id>
<article-id pub-id-type="doi">10.1016/bs.aivir.2019.08.002</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Structural insights into coronavirus entry</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" id="au0010"><name><surname>Tortorici</surname>
<given-names>M. Alejandra</given-names>
</name>
<xref rid="af0010" ref-type="aff">a</xref>
<xref rid="af0015" ref-type="aff">b</xref>
<xref rid="af0020" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author" id="au0015"><name><surname>Veesler</surname>
<given-names>David</given-names>
</name>
<email>dveesler@uw.edu</email>
<xref rid="af0010" ref-type="aff">a</xref>
<xref rid="cr0010" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af0010"><label>a</label>
Department of Biochemistry, University of Washington, Seattle, WA, United States</aff>
<aff id="af0015"><label>b</label>
Institut Pasteur, Unité de Virologie Structurale, Paris, France</aff>
<aff id="af0020"><label>c</label>
CNRS UMR 3569, Unité de Virologie Structurale, Paris, France</aff>
<author-notes><corresp id="cr0010"><label>*</label>
Corresponding author: <email>dveesler@uw.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>22</day>
<month>8</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>22</day>
<month>8</month>
<year>2019</year>
</pub-date>
<volume>105</volume>
<fpage>93</fpage>
<lpage>116</lpage>
<permissions><copyright-statement>Copyright © 2019 Elsevier Inc. All rights reserved.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Elsevier Inc.</copyright-holder>
<license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p>
</license>
</permissions>
<abstract id="ab0010"><p>Coronaviruses (CoVs) have caused outbreaks of deadly pneumonia in humans since the beginning of the 21st century. The severe acute respiratory syndrome coronavirus (SARS-CoV) emerged in 2002 and was responsible for an epidemic that spread to five continents with a fatality rate of 10% before being contained in 2003 (with additional cases reported in 2004). The Middle-East respiratory syndrome coronavirus (MERS-CoV) emerged in the Arabian Peninsula in 2012 and has caused recurrent outbreaks in humans with a fatality rate of 35%. SARS-CoV and MERS-CoV are zoonotic viruses that crossed the species barrier using bats/palm civets and dromedary camels, respectively. No specific treatments or vaccines have been approved against any of the six human coronaviruses, highlighting the need to investigate the principles governing viral entry and cross-species transmission as well as to prepare for zoonotic outbreaks which are likely to occur due to the large reservoir of CoVs found in mammals and birds. Here, we review our understanding of the infection mechanism used by coronaviruses derived from recent structural and biochemical studies.</p>
</abstract>
<kwd-group id="ks0010"><title>Keywords</title>
<kwd>Coronavirus</kwd>
<kwd>Spike glycoprotein</kwd>
<kwd>Fusion protein</kwd>
<kwd>Membrane fusion</kwd>
<kwd>Proteolytic activation</kwd>
<kwd>Vaccine design</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec id="no0010"><title>Abbreviations</title>
<def-list><def-item><term id="dt0010">3D</term>
<def><p id="p0010">three dimensional</p>
</def>
</def-item>
<def-item><term id="dt0015">9-<italic>O</italic>
-Ac-Sia</term>
<def><p id="p0015">5-<italic>N</italic>
-acetyl-9-<italic>O</italic>
-acetyl-sialosides</p>
</def>
</def-item>
<def-item><term id="dt0020">ACE2</term>
<def><p id="p0020">angiotensin-converting enzyme 2</p>
</def>
</def-item>
<def-item><term id="dt0025">APN</term>
<def><p id="p0025">amino-peptidase N</p>
</def>
</def-item>
<def-item><term id="dt0030">CoV</term>
<def><p id="p0030">Coronavirus</p>
</def>
</def-item>
<def-item><term id="dt0035">cryoEM</term>
<def><p id="p0035">cryo-electron microscopy</p>
</def>
</def-item>
<def-item><term id="dt0040">DPP4</term>
<def><p id="p0040">dipeptidyl peptidase 4</p>
</def>
</def-item>
<def-item><term id="dt0045">Fab</term>
<def><p id="p0045">antigen-binding fragment of an antibody</p>
</def>
</def-item>
<def-item><term id="dt0050">MERS-CoV</term>
<def><p id="p0050">Middle-East respiratory syndrome coronavirus</p>
</def>
</def-item>
<def-item><term id="dt0055">MHV</term>
<def><p id="p0055">mouse hepatitis virus</p>
</def>
</def-item>
<def-item><term id="dt0060">PDCoV</term>
<def><p id="p0060">porcine δ-CoV</p>
</def>
</def-item>
<def-item><term id="dt0065">PEDV</term>
<def><p id="p0065">porcine epidemic diarrhea virus</p>
</def>
</def-item>
<def-item><term id="dt0070">SARS-CoV</term>
<def><p id="p0070">severe acute respiratory syndrome coronavirus</p>
</def>
</def-item>
<def-item><term id="dt0075">TGEV</term>
<def><p id="p0075">transmissible gastroenteritis virus</p>
</def>
</def-item>
</def-list>
</sec>
<sec id="s0010"><label>1</label>
<title>Introduction</title>
<p id="p0080">Coronaviruses (CoVs) are enveloped viruses with a positive sense RNA genome, that belong to the subfamily <italic>Coronavirinae</italic>
within the family <italic>Coronaviridae</italic>
, which is part of the Nidovirales order. They are classified in four genera (α, β, γ, and δ) and four lineages are recognized whithin the β-CoV genus (A, B, C and D). CoVs cause a variety of respiratory and enteric diseases in mammalian and avian species. Until recently, CoVs were considered to be pathogens with a largely veterinary relevance but with limited impact on human health. However, outbreaks of severe acute respiratory syndrome (SARS) in 2002–2004 and of Middle-East respiratory syndrome (MERS) starting in 2012, with fatality rates of 10% and 35%, respectively, led CoVs to be recognized as zoonotic threats with pandemic potential. Four other CoVs are endemic in the human population and cause up to 30% of mild respiratory tract infections as well as occasional severe disease in young children, the elderly or immunocompromised individuals (<xref rid="bb0220" ref-type="bibr">Isaacs et al., 1983</xref>
; <xref rid="bb0480" ref-type="bibr">Su et al., 2016</xref>
). These viruses are HCoV-NL63 and HCoV-229E (α-CoVs) as well as HCoV-OC43 and HCoV-HKU1 (β-CoVs). Numerous SARS-CoV and MERS-CoV-like viruses currently circulate in bats and dromedaries making outbreaks of highly pathogenic human CoVs a global health threat (<xref rid="bb0170" ref-type="bibr">Ge et al., 2013</xref>
; <xref rid="bb0180" ref-type="bibr">Haagmans et al., 2014</xref>
; <xref rid="bb0200" ref-type="bibr">Hu et al., 2017</xref>
; <xref rid="bb0325" ref-type="bibr">Menachery et al., 2015</xref>
, <xref rid="bb0330" ref-type="bibr">Menachery et al., 2016</xref>
; <xref rid="bb0430" ref-type="bibr">Sabir et al., 2016</xref>
).</p>
<p id="p0085">The CoV virion contains at least four structural proteins: spike (S), envelope (E), membrane (M) and nucleocapsid (N). In contrast to other β-CoV lineages, lineage A CoVs also encode a hemagglutinin–esterase which serves as receptor-destroying enzyme to facilitate release of viral progeny from infected cells and escape from attachment to non-permissive host cells or decoys (<xref rid="bb0015" ref-type="bibr">Bakkers et al., 2017</xref>
, <xref rid="bb0020" ref-type="bibr">Bakkers et al., 2016</xref>
). S is a class 1 viral fusion protein that promotes host attachment and fusion of the viral and cellular membranes during entry (<xref rid="bb0060" ref-type="bibr">Bosch et al., 2003</xref>
). As a consequence, S determines host range and cell tropism. S is also the main target of neutralizing antibodies elicited during infection and the focus of vaccine design. S is trimeric and each protomer is synthesized as a single polypeptide chain of 1100–1600 residues, depending on the CoV species. For many CoVs, S is processed by host proteases to generate two functional subunits, designated S<sub>1</sub>
and S<sub>2</sub>
, which remain non-covalently bound in the prefusion conformation (<xref rid="bb0060" ref-type="bibr">Bosch et al., 2003</xref>
). The S<sub>1</sub>
subunit comprises the apex of the S trimer, including the receptor-binding domains, and stabilizes the prefusion state of the S<sub>2</sub>
fusion machinery, which is anchored in the viral membrane. For all CoVs, S is further cleaved by host proteases at the so-called S<sub>2</sub>
’ site located immediately upstream of the fusion peptide. This cleavage has been proposed to activate the protein for membrane fusion <italic>via</italic>
large-scale, irreversible conformational changes (<xref rid="bb0190" ref-type="bibr">Heald-Sargent and Gallagher, 2012</xref>
; <xref rid="bb0345" ref-type="bibr">Millet and Whittaker, 2015</xref>
).</p>
<p id="p0090">Although several class 1 viral fusion proteins have been extensively studied, CoV S proteins have proven reluctant to structural characterization until recently. Structural studies were largely limited to X-ray crystallographic analysis of isolated receptor-binding domains in complex with viral receptor ectodomains or neutralizing antibodies (<xref rid="bb0260" ref-type="bibr">Li et al., 2005a</xref>
; <xref rid="bb0305" ref-type="bibr">Lu et al., 2013</xref>
; <xref rid="bb0375" ref-type="bibr">Peng et al., 2011</xref>
; <xref rid="bb0390" ref-type="bibr">Prabakaran et al., 2006</xref>
; <xref rid="bb0410" ref-type="bibr">Reguera et al., 2012</xref>
; <xref rid="bb0550" ref-type="bibr">Wang et al., 2013</xref>
; <xref rid="bb0580" ref-type="bibr">Wong et al., 2017</xref>
; <xref rid="bb0590" ref-type="bibr">Wu et al., 2009</xref>
; <xref rid="bb0655" ref-type="bibr">Yu et al., 2015</xref>
) and of the S<sub>2</sub>
postfusion core (<xref rid="bb0135" ref-type="bibr">Duquerroy et al., 2005</xref>
; <xref rid="bb0165" ref-type="bibr">Gao et al., 2013</xref>
; <xref rid="bb0485" ref-type="bibr">Supekar et al., 2004</xref>
; <xref rid="bb0610" ref-type="bibr">Xu et al., 2004a</xref>
, <xref rid="bb0615" ref-type="bibr">Xu et al., 2004b</xref>
; <xref rid="bb0670" ref-type="bibr">Zheng et al., 2006</xref>
) with the exception of two low-resolution electron microscopy reports (<xref rid="bb0035" ref-type="bibr">Beniac et al., 2006</xref>
, <xref rid="bb0040" ref-type="bibr">Beniac et al., 2007</xref>
). In the past few years, however, technical advances in single-particle cryo-electron microscopy (cryoEM) (<xref rid="bb0010" ref-type="bibr">Bai et al., 2013</xref>
; <xref rid="bb0065" ref-type="bibr">Brilot et al., 2012</xref>
; <xref rid="bb0075" ref-type="bibr">Campbell et al., 2012</xref>
, <xref rid="bb0080" ref-type="bibr">Campbell et al., 2015</xref>
; <xref rid="bb0290" ref-type="bibr">Li et al., 2013</xref>
; <xref rid="bb0395" ref-type="bibr">Punjani et al., 2017</xref>
; <xref rid="bb0435" ref-type="bibr">Scheres, 2012</xref>
) together with the implementation of strategies for the stabilization of CoV S proteins in prefusion conformation (<xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
; <xref rid="bb0525" ref-type="bibr">Walls et al., 2017a</xref>
) led to a surge of structural data for multiple S ectodomain trimers. We review here our current understanding of the mechanism used by CoVs to infect host cells based on recent structural and biochemical studies of S glycoprotein ectodomains in prefusion and postfusion states as well as complexes with known receptors or neutralizing antibodies.</p>
</sec>
<sec id="s0015"><label>2</label>
<title>Prefusion S architecture</title>
<p id="p0095">CryoEM studies of the S glycoproteins of mouse hepatitis virus (MHV) and HKU1 led to the first structures at high-enough resolution to obtain an atomic model of the prefusion state (<xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
). These structures revealed that prefusion S ectodomains are ~ 160 Å-long trimers with a triangular cross-section (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
A and B).<fig id="f0010"><label>Fig. 1</label>
<caption><p>CryoEM structure of the apo-HCoV-OC43 S glycoprotein. (A) Ribbon diagrams of the apo HCoV-OC43 S ectodomain trimer (PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6OHW" id="ir0010">6OHW</ext-link>
) in two orthogonal orientations, from the side (left) and from the top, looking towards the viral membrane (right). (B) Side view of one S protomer. (C) Ribbon diagram of the HCoV-OC43 S<sub>1</sub>
subunit. (D–E) Close-up view of HCoV-OC43 domain A (D) and domain B (E). (F) Ribbon diagram of the HCoV-OC43 S<sub>2</sub>
subunit in the prefusion conformation. The N- and C-termini are labeled in panels (B–E).</p>
</caption>
<alt-text id="al0010">Fig. 1</alt-text>
<graphic xlink:href="f04-01-9780128184561_lrg"></graphic>
</fig>
</p>
<p id="p0100">The S<sub>1</sub>
subunit adopts a “V” shaped architecture for β and γ CoVs (<xref rid="bb0175" ref-type="bibr">Gui et al., 2017</xref>
; <xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0450" ref-type="bibr">Shang et al., 2018a</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
; <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
) (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
C), or a square-shaped organization for α- and δ-CoVs (<xref rid="bb0455" ref-type="bibr">Shang et al., 2018b</xref>
; <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
). The S<sub>1</sub>
subunit folds as β-rich domains designated A, B, C, D. Several α-CoVs harbor a likely duplication of their domain A at the N-terminus of the S glycoprotein (<xref rid="bb0205" ref-type="bibr">Hulswit et al., 2016</xref>
; <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
). This additional domain, designated domain 0, was visualized in the NL63 S structure and hypothesized to interact with heparan sulfate present at the host cell surface during viral entry (<xref rid="bb0335" ref-type="bibr">Milewska et al., 2014</xref>
; <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
). Domain A and domain 0 adopt a galectin-like β-sandwich fold conserved across all CoV genera (<xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0375" ref-type="bibr">Peng et al., 2011</xref>
, <xref rid="bb0380" ref-type="bibr">Peng et al., 2012</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
) (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
D). Domain B, which shows the highest sequence variability within CoV S<sub>1</sub>
subunits, has a markedly different architecture between α-, β-, γ- and δ-CoVs. B domains of β-CoVs contain a β-sheet core subdomain decorated with a highly variable external subdomain mediating receptor engagement (<xref rid="bb0095" ref-type="bibr">Chen et al., 2013</xref>
; <xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0285" ref-type="bibr">Li et al., 2005b</xref>
; <xref rid="bb0305" ref-type="bibr">Lu et al., 2013</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
; <xref rid="bb0550" ref-type="bibr">Wang et al., 2013</xref>
) (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
E). B domains of α-, γ- and δ-CoV form a β-sandwich decorated with loops mediating receptor attachment (<xref rid="bb0410" ref-type="bibr">Reguera et al., 2012</xref>
; <xref rid="bb0450" ref-type="bibr">Shang et al., 2018a</xref>
, <xref rid="bb0455" ref-type="bibr">Shang et al., 2018b</xref>
; <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0580" ref-type="bibr">Wong et al., 2017</xref>
; <xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
). In the context of the S trimer, β/γ CoV B domains interact with the A and B domains of another protomer, whereas they pack against the A domain of the same protomer in α/δ-CoVs (<xref rid="bb0450" ref-type="bibr">Shang et al., 2018a</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
, <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
).</p>
<p id="p0105">The S<sub>2</sub>
subunit, which is more conserved than S<sub>1</sub>
, comprises the fusion machinery and connects to the viral membrane. It is assembled from a large number of α-helices, an antiparallel core β-sheet, a β-rich connector domain and a stem helix leading to the heptad-repeat 2 (HR2) and the transmembrane region (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
F) (<xref rid="bb0175" ref-type="bibr">Gui et al., 2017</xref>
; <xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
, <xref rid="bb0230" ref-type="bibr">Kirchdoerfer et al., 2018</xref>
; <xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
; <xref rid="bb0450" ref-type="bibr">Shang et al., 2018a</xref>
, <xref rid="bb0455" ref-type="bibr">Shang et al., 2018b</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
, <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
, <xref rid="bb0540" ref-type="bibr">Walls et al., 2017b</xref>
; <xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
; <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
). Key S<sub>2</sub>
features facilitating virus-cell fusion include the fusion peptide, two heptad repeat regions (named HR1 and HR2) and the transmembrane domain. In the prefusion S conformation, a central helix stretches along the threefold axis, perpendicular to the viral membrane, and is located downstream the HR1 motif, which folds as four consecutive α-helices (<xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
). Moreover, an upstream helix runs parallel to and is zipped against the central helix <italic>via</italic>
hydrophobic contacts (<xref rid="f0010" ref-type="fig">Fig. 1</xref>
F). The CoV S<sub>2</sub>
subunit shares similarity with the pneumovirus/paramyxovirus F proteins—including a comparable 3D organization of the core β-sheet, the upstream helix and the central helix—suggesting an evolutionary relatedness between the viral fusion proteins of these different viruses and a conservation of their fusion mechanism (<xref rid="bb0315" ref-type="bibr">McLellan et al., 2013</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
, <xref rid="bb0540" ref-type="bibr">Walls et al., 2017b</xref>
; <xref rid="bb0585" ref-type="bibr">Wong et al., 2016</xref>
; <xref rid="bb0605" ref-type="bibr">Xu et al., 2015</xref>
; <xref rid="bb0645" ref-type="bibr">Yin et al., 2006</xref>
).</p>
<p id="p0110">A conserved tryptophan-rich segment (Y(V/I)KWPW(Y/W)VWL) directly preceding the CoV S transmembrane region is crucial for proper trimerization. This segment is also required functionally for formation of a fusion pore (<xref rid="bb0440" ref-type="bibr">Schroth-Diez et al., 2000</xref>
). Furthermore, transmembrane domain interactions within and possibly between S trimers have been proposed to be essential to complete the membrane fusion process (<xref rid="bb0440" ref-type="bibr">Schroth-Diez et al., 2000</xref>
). The transmembrane domain is followed by an intraviral/cytoplasmic tail of variable length (36–46 residues) depending on the coronavirus species, which contains a palmitoylated cysteine-rich region (of about 18–24 residues with 7–10 cysteines) and a variable C-terminal end (<xref rid="bb0500" ref-type="bibr">Thorp et al., 2006</xref>
). The cytoplasmic tail is involved in assembly, intracellular transport, cell-surface expression and cell-cell fusion (<xref rid="bb0045" ref-type="bibr">Bos et al., 1995</xref>
; <xref rid="bb0055" ref-type="bibr">Bosch et al., 2005</xref>
; <xref rid="bb0085" ref-type="bibr">Chang et al., 2000</xref>
; <xref rid="bb0300" ref-type="bibr">Lontok et al., 2004</xref>
; <xref rid="bb0385" ref-type="bibr">Petit et al., 2005</xref>
; <xref rid="bb0630" ref-type="bibr">Ye et al., 2004</xref>
; <xref rid="bb0650" ref-type="bibr">Youn et al., 2005</xref>
). Currently, no structural information is available for any CoV full-length S, hindering our understanding of the influence of the transmembrane and cytoplasmic domains on the conformation of exposed antigenic sites, as previously studied for HIV-1 envelope (<xref rid="bb0090" ref-type="bibr">Chen et al., 2015</xref>
;<xref rid="bb0125" ref-type="bibr">Dev et al., 2016</xref>
).</p>
</sec>
<sec id="s0020"><label>3</label>
<title>Diversity of CoV receptors and entry mechanisms</title>
<p id="p0115">CoV entry into susceptible cells is a complex process that requires the concerted action of receptor-binding and proteolytic processing of the S protein to promote virus-cell fusion (<xref rid="bb0190" ref-type="bibr">Heald-Sargent and Gallagher, 2012</xref>
; <xref rid="bb0345" ref-type="bibr">Millet and Whittaker, 2015</xref>
). Domain 0, domain A and/or domain B can act as receptor-binding domains and both attachment and entry receptors have been described, depending on the CoV species.</p>
<p id="p0120">Lineage A β-CoVs attach <italic>via</italic>
their S domain A to 5-<italic>N</italic>
-acetyl-9-<italic>O</italic>
-acetyl-sialosides (9-<italic>O</italic>
-Ac-Sia) found on glycoproteins and glycolipids at the host cell surface to promote entry into susceptible cells (<xref rid="bb0520" ref-type="bibr">Vlasak et al., 1988</xref>
). These include human CoVs OC43 and HKU1, bovine CoV (BCoV) and porcine hemagglutinating encephalomyelitis virus. We recently identified and visualized by cryoEM the HCoV-OC43 S sialoside-binding site, which is located in a groove at the surface of domain A (<xref rid="f0015" ref-type="fig">Fig. 2</xref>
A) (<xref rid="bb0210" ref-type="bibr">Hulswit et al., 2019</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
). This site is conserved in all other CoVs known to attach to 9-<italic>O</italic>
-Ac-Sia (β-CoVs, lineage A) and shares architectural similarity with the ligand-binding pockets of CoV hemagglutinin-esterases and influenza virus C/D hemagglutinin-esterase-fusion glycoproteins, highlighting common structural principles of recognition (<xref rid="bb0015" ref-type="bibr">Bakkers et al., 2017</xref>
, <xref rid="bb0020" ref-type="bibr">Bakkers et al., 2016</xref>
; <xref rid="bb0210" ref-type="bibr">Hulswit et al., 2019</xref>
; <xref rid="bb0425" ref-type="bibr">Rosenthal et al., 1998</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
). The current consensus in the field is that HCoV-OC43 only utilizes 9-<italic>O</italic>
-Ac-sialosides as host receptors. In line with this statement, ligand-interacting residues were shown to be essential for S-mediated viral entry (<xref rid="bb0210" ref-type="bibr">Hulswit et al., 2019</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
) and 9-<italic>O</italic>
-Ac-Sia depletion from target cells resulted in severe decrease in virus infectivity (<xref rid="bb0240" ref-type="bibr">Krempl et al., 1995</xref>
; <xref rid="bb0520" ref-type="bibr">Vlasak et al., 1988</xref>
). Free 9-<italic>O</italic>
-Ac-Sia, however, did not trigger S conformational changes associated with membrane fusion (<xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
). This observation contrasts with data for SARS-CoV S, for which addition of the human angiotensin-converting enzyme 2 (ACE2) ectodomain (the proteinaceous receptor) promoted S refolding to the postfusion state (<xref rid="bb0470" ref-type="bibr">Song et al., 2018</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
). These findings suggested that either 9-<italic>O</italic>
-Ac-Sia-containing receptors differ from proteinaceous receptors in their mode of action, or that an interaction with a yet unidentified proteinaceous receptor is required before or after virus internalization for HCoV-OC43 entry into target cells.<fig id="f0015"><label>Fig. 2</label>
<caption><p>Structural studies of human CoV attachment to host receptors. (A–E), Ribbon diagrams of the complex between domain A of HCoV-OC43 S with a 9-<italic>O</italic>
-Ac-Sia receptor analogue ((A) PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6NZK" id="ir0015">6NZK</ext-link>
), or the domain B of SARS-CoV S with ACE2 ((B) PDB: <ext-link ext-link-type="uri" xlink:href="pdb:2AJF" id="ir0020">2AJF</ext-link>
), HCoV-NL63 S with ACE2 ((C) PDB: <ext-link ext-link-type="uri" xlink:href="pdb:3KBH" id="ir0025">3KBH</ext-link>
), MERS-CoV S with DPP4 ((D) PDB: <ext-link ext-link-type="uri" xlink:href="pdb:4L72" id="ir0030">4L72</ext-link>
) and HCoV-229E S with APN ((E) PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6ATK" id="ir0035">6ATK</ext-link>
). In panels (B–E), each domain B is rendered in light blue and the receptor binding-motifs are colored purple.</p>
</caption>
<alt-text id="al0015">Fig. 2</alt-text>
<graphic xlink:href="f04-02-9780128184561_lrg"></graphic>
</fig>
</p>
<p id="p0125">The sialoside-binding site identified in HCoV-OC43 S is not conserved among CoVs which are also known to interact with sialoglycans to initiate host cell infection but are outside of the lineage A of β-CoVs, such as MERS-CoV (β-CoV, lineage C) or infectious bronchitis virus (IBV, δ-CoV) (<xref rid="bb0270" ref-type="bibr">Li et al., 2017</xref>
; <xref rid="bb0570" ref-type="bibr">Wickramasinghe et al., 2011</xref>
). Some α-CoVs such as transmissible gastroenteritis virus (TGEV) and porcine epidemic diarrhea virus (PEDV) use domain 0 to attach to sialoglycans, presumably to increase virus concentration at the cell surface and enhance subsequent attachment to proteinaceous receptors (<xref rid="bb0295" ref-type="bibr">Liu et al., 2015</xref>
; <xref rid="bb0445" ref-type="bibr">Schwegmann-Wessels et al., 2003</xref>
). Carbohydrate binding <italic>via</italic>
this domain has been proposed to be a determinant of the TGEV enteric tropism since loss of domain 0 appears to correlate with a loss of enteric tropism for porcine respiratory coronavirus (PRCoV), the latter virus being a naturally occurring TGEV variant (<xref rid="bb0245" ref-type="bibr">Krempl et al., 1997</xref>
).</p>
<p id="p0130">CoVs exploit a limited variety of proteinaceous receptors compared with the large number and diversity of viral species. All CoVs known to engage proteinaceous receptors do so using domain B with the exception of MHV, which binds CEACAM1a using domain A (<xref rid="bb0140" ref-type="bibr">Dveksler et al., 1991</xref>
; <xref rid="bb0375" ref-type="bibr">Peng et al., 2011</xref>
; <xref rid="bb0575" ref-type="bibr">Williams et al., 1991</xref>
). Remarkably, viruses from different genera, such as HCoV-NL63 (α-CoV) and SARS-CoV (β-CoV), can recognize the same region of ACE2 (entry receptor) using structurally distinct B domains (<xref rid="bb0195" ref-type="bibr">Hofmann et al., 2005</xref>
; <xref rid="bb0260" ref-type="bibr">Li et al., 2005a</xref>
, <xref rid="bb0275" ref-type="bibr">Li et al., 2003</xref>
; <xref rid="bb0590" ref-type="bibr">Wu et al., 2009</xref>
). Many α-CoVs, including HCoV-229E, TGEV and PRCV, as well as porcine δ-CoV (PDCoV) utilize aminopeptidase N (APN) as entry receptor (<xref rid="bb0115" ref-type="bibr">Delmas et al., 1992</xref>
; <xref rid="bb0120" ref-type="bibr">Delmas et al., 1993</xref>
; <xref rid="bb0265" ref-type="bibr">Li et al., 2018</xref>
; <xref rid="bb0410" ref-type="bibr">Reguera et al., 2012</xref>
; <xref rid="bb0580" ref-type="bibr">Wong et al., 2017</xref>
; <xref rid="bb0635" ref-type="bibr">Yeager et al., 1992</xref>
) whereas MERS-CoV uses dipeptidyl peptidase 4 (DPP4) (<xref rid="bb0305" ref-type="bibr">Lu et al., 2013</xref>
; <xref rid="bb0400" ref-type="bibr">Raj et al., 2013</xref>
; <xref rid="bb0550" ref-type="bibr">Wang et al., 2013</xref>
). Crystal structures of SARS-CoV, HCoV-NL63, MERS-CoV, HCoV-229E B domains in complex with their cognate receptors provided atomic details of the interacting-interface and identified key residues for cross-species transmission and infection (<xref rid="f0015" ref-type="fig">Fig. 2</xref>
) (<xref rid="bb0260" ref-type="bibr">Li et al., 2005a</xref>
; <xref rid="bb0305" ref-type="bibr">Lu et al., 2013</xref>
; <xref rid="bb0550" ref-type="bibr">Wang et al., 2013</xref>
; <xref rid="bb0580" ref-type="bibr">Wong et al., 2017</xref>
; <xref rid="bb0590" ref-type="bibr">Wu et al., 2009</xref>
). This information will be useful to guide the development of therapeutics and vaccines against human CoVs.</p>
<p id="p0135">Recent cryoEM studies revealed that MERS-CoV S and SARS-CoV S can adopt open and closed conformations in which the receptor binding site of domain B is exposed and occluded, respectively (<xref rid="bb0175" ref-type="bibr">Gui et al., 2017</xref>
; <xref rid="bb0230" ref-type="bibr">Kirchdoerfer et al., 2018</xref>
; <xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
; <xref rid="bb0470" ref-type="bibr">Song et al., 2018</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
; <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
). In contrast, the MHV, HCoV-NL63, HCoV-HKU1, PDCoV, IBV and HCoV-OC43 S glycoproteins appear to only adopt a closed conformation (<xref rid="bb0225" ref-type="bibr">Kirchdoerfer et al., 2016</xref>
; <xref rid="bb0450" ref-type="bibr">Shang et al., 2018a</xref>
, <xref rid="bb0455" ref-type="bibr">Shang et al., 2018b</xref>
; <xref rid="bb0505" ref-type="bibr">Tortorici et al., 2019</xref>
; <xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
, <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
) and unknown trigger(s), besides proteolytic activation, might be necessary for these viruses to expose their receptor-binding motifs for recognition to occur. These findings suggest that CoVs have evolved a fine-tuned mechanism to balance masking of the receptor-binding motifs, putatively to avoid neutralization by the host humoral immune response, and their necessary exposure to enable receptor recognition and infection of host cells (<xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
, <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
; <xref rid="bb0580" ref-type="bibr">Wong et al., 2017</xref>
).</p>
<p id="p0140">Upon host recognition, CoVs are internalized <italic>via</italic>
receptor-mediated clathrin-dependent, caveolin-dependent or other uptake pathways (<xref rid="bb0070" ref-type="bibr">Burkard et al., 2014</xref>
; <xref rid="bb0155" ref-type="bibr">Eifart et al., 2007</xref>
; <xref rid="bb0215" ref-type="bibr">Inoue et al., 2007</xref>
; <xref rid="bb0355" ref-type="bibr">Nomura et al., 2004</xref>
). For instance, both clathrin-dependent and clathrin/caveolae-independent entry pathways have been reported for SARS-CoV (<xref rid="bb0215" ref-type="bibr">Inoue et al., 2007</xref>
; <xref rid="bb0560" ref-type="bibr">Wang et al., 2008</xref>
). Feline infectious peritonitis virus was suggested to enter host cells <italic>via</italic>
a clathrin/caveolin-independent internalization route (<xref rid="bb0405" ref-type="bibr">Regan et al., 2008</xref>
; <xref rid="bb0515" ref-type="bibr">Van Hamme et al., 2008</xref>
) whereas a caveolin-dependent endocytic uptake has been suggested for HCoV-229E and HCoV-OC43 (<xref rid="bb0355" ref-type="bibr">Nomura et al., 2004</xref>
; <xref rid="bb0360" ref-type="bibr">Owczarek et al., 2018</xref>
).</p>
</sec>
<sec id="s0025"><label>4</label>
<title>S proteolytic cleavage</title>
<p id="p0145">Several reports have demonstrated the key role of proteolytic processing of CoV S for cell-cell fusion activity and/or virus entry into host cells using experiments of inhibition of intracellular proteases (<xref rid="bb0070" ref-type="bibr">Burkard et al., 2014</xref>
; <xref rid="bb0160" ref-type="bibr">Frana et al., 1985</xref>
; <xref rid="bb0465" ref-type="bibr">Simmons et al., 2005</xref>
; <xref rid="bb0620" ref-type="bibr">Yamada and Liu, 2009</xref>
) and/or substitutions of residues at the S<sub>1</sub>
/S<sub>2</sub>
or S<sub>2</sub>
’ cleavage sites (<xref rid="bb0030" ref-type="bibr">Belouzard et al., 2009</xref>
; <xref rid="bb0280" ref-type="bibr">Li et al., 2015</xref>
; <xref rid="bb0340" ref-type="bibr">Millet and Whittaker, 2014</xref>
; <xref rid="bb0565" ref-type="bibr">Wicht et al., 2014</xref>
; <xref rid="bb0625" ref-type="bibr">Yang et al., 2015</xref>
).</p>
<p id="p0150">Prior to and/or after uptake of the virion by a host cell, the S protein is proteolytically processed by host proteases at one or two cleavage sites and both receptor-binding and proteolytic processing act in synergy to induce large-scale S conformational changes promoting CoV entry. One of the cleavage sites is located at the boundary between the S<sub>1</sub>
and S<sub>2</sub>
subunits (S<sub>1</sub>
/S<sub>2</sub>
cleavage site), whereas the other is located immediately upstream of the fusion peptide (S<sub>2</sub>
’ cleavage site), reviewed in (<xref rid="bb0345" ref-type="bibr">Millet and Whittaker, 2015</xref>
). Cleavage at the S<sub>1</sub>
/S<sub>2</sub>
site can occur upon viral egress, such as for MHV (<xref rid="bb0160" ref-type="bibr">Frana et al., 1985</xref>
), or upon encounter with a target cell, such as for SARS-CoV (<xref rid="bb0030" ref-type="bibr">Belouzard et al., 2009</xref>
; <xref rid="bb0050" ref-type="bibr">Bosch et al., 2008</xref>
; <xref rid="bb0460" ref-type="bibr">Shulla et al., 2011</xref>
), to yield two non-covalently associated subunits. This first cleavage event, along with binding to the host receptor, promotes further cleavage at the S<sub>2</sub>
’ site for SARS-CoV S (<xref rid="bb0030" ref-type="bibr">Belouzard et al., 2009</xref>
) and MERS-CoV S (<xref rid="bb0340" ref-type="bibr">Millet and Whittaker, 2014</xref>
;<xref rid="bb0370" ref-type="bibr">Park et al., 2016</xref>
). Proteolysis at the conserved S<sub>2</sub>
’ site is essential for fusion activation of all characterized CoV S proteins, and it can occur at the host membrane or in internal cellular compartments of the target cell (<xref rid="bb0030" ref-type="bibr">Belouzard et al., 2009</xref>
; <xref rid="bb0070" ref-type="bibr">Burkard et al., 2014</xref>
; <xref rid="bb0345" ref-type="bibr">Millet and Whittaker, 2015</xref>
; <xref rid="bb0370" ref-type="bibr">Park et al., 2016</xref>
).</p>
<p id="p0155">Cleavage at the MERS-CoV S<sub>1</sub>
/S<sub>2</sub>
site by furin during viral egress enables subsequent exposure of the S<sub>2</sub>
’ site upon binding to the host receptor and a second cleavage step by serine proteases anchored in the membrane of the target cells, eventually leading to fusion at the cytoplasmic membrane (early entry) (<xref rid="bb0370" ref-type="bibr">Park et al., 2016</xref>
). Conversely, MERS-CoV budding with uncleaved S glycoproteins traffic to the endosomes of target cells where cathepsin L or other proteases promote membrane fusion (late entry) (<xref rid="bb0370" ref-type="bibr">Park et al., 2016</xref>
). The former mechanism has been proposed to be the route of MERS-CoV entry into cell types relevant to lung infection, and therefore a significant determinant of MERS-CoV virulence (<xref rid="bb0370" ref-type="bibr">Park et al., 2016</xref>
). Moreover, tetraspanin CD9 has been implicated in clustering DPP4 and transmembrane serine proteases to promote early entry of MERS-CoV (<xref rid="bb0145" ref-type="bibr">Earnest et al., 2017</xref>
, <xref rid="bb0150" ref-type="bibr">Earnest et al., 2015</xref>
). PEDV, which replicates in the epithelial cells of the small intestine, undergoes S proteolytic activation by trypsin, which is highly abundant in the intestinal lumen (<xref rid="bb0565" ref-type="bibr">Wicht et al., 2014</xref>
). The critical importance of cleavage at the S<sub>1</sub>
/S<sub>2</sub>
site was also exemplified in studies with the MERS-CoV-related bat coronavirus HKU4. Although HKU4 S recognizes human DPP4, <italic>in vitro</italic>
infectivity assays revealed that entry into human cells required addition of exogenous trypsin, suggesting proteolytic activation of this bat virus did not occur in human cells (<xref rid="bb0555" ref-type="bibr">Wang et al., 2014</xref>
). In line with these findings, various DPP4 mammalian orthologues, with variable binding affinities for the MERS-CoV S receptor-binding domain, were shown to support virus or pseudovirus entry into target cells in the presence of an activating protease (<xref rid="bb0025" ref-type="bibr">Barlan et al., 2014</xref>
). These results collectively illustrate how specific S proteolytic cleavage participates in determining the intracellular site of fusion and also viral tropism and pathogenesis of CoVs. Therefore, the zoonotic potential of CoVs is not only determined by receptor engagement, but also by proteolytic processing of the S protein required for fusion activation.</p>
</sec>
<sec id="s0030"><label>5</label>
<title>Mechanism of fusion activation</title>
<p id="p0160">We showed that <italic>in vitro</italic>
trypsin cleavage of MHV, SARS-CoV and MERS-CoV S, under limited proteolysis conditions, recapitulated fusion activation by inducing the pre-to postfusion transition (<xref rid="bb0540" ref-type="bibr">Walls et al., 2017b</xref>
). The cryoEM structure of the MHV S<sub>2</sub>
subunit ectodomain trimer revealed that membrane fusion involves large-scale S conformational changes that are reminiscent of the ones described for other class 1 fusion proteins, including the pneumovirus/paramyxovirus F glycoproteins (<xref rid="f0020" ref-type="fig">Fig. 3</xref>
) (<xref rid="bb0320" ref-type="bibr">McLellan et al., 2011</xref>
; <xref rid="bb0490" ref-type="bibr">Swanson et al., 2010</xref>
, <xref rid="bb0495" ref-type="bibr">Swanson et al., 2011</xref>
; <xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0640" ref-type="bibr">Yin et al., 2005</xref>
). These experiments also demonstrated that (i) the S<sub>1</sub>
subunits stabilize the S<sub>2</sub>
fusion machinery in the spring-loaded, metastable prefusion state before initiation of infection; and (ii) postfusion S is the ground state of the fusion reaction. Similarly to the organization of influenza virus hemagglutinins (<xref rid="bb0595" ref-type="bibr">Xiong et al., 2013</xref>
), domain B interacts with the HR1-central helix hairpin in prefusion closed S structures likely to stabilize S<sub>2</sub>
in the spring-loaded prefusion state. This interaction appears to coordinate receptor engagement with fusion. Upon receptor binding and proteolytic cleavage at the S<sub>1</sub>
/S<sub>2</sub>
and S<sub>2</sub>
′ sites, the S<sub>1</sub>
crown is likely shed (as observed for MERS-CoV S by <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
) to facilitate a conformational change of S<sub>2</sub>
, which involves projection of the fusion peptide to a distance of ~ 100 Å and its insertion into the target membrane (<xref rid="f0020" ref-type="fig">Fig. 3</xref>
) (<xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
, <xref rid="bb0540" ref-type="bibr">Walls et al., 2017b</xref>
). The free energy released upon S<sub>2</sub>
refolding from the prefusion to the postfusion state is believed to bring the viral and host membranes in close proximity and promote membrane merger (<xref rid="bb0185" ref-type="bibr">Harrison, 2008</xref>
).<fig id="f0020"><label>Fig. 3</label>
<caption><p>CoV S conformational changes driving the fusion reaction. (A), Ribbon diagram of the MHV S<sub>2</sub>
subunit in the prefusion conformation, PDB: <ext-link ext-link-type="uri" xlink:href="pdb:3JCL" id="ir0040">3JCL</ext-link>
. (B), Ribbon diagram of the MHV S<sub>2</sub>
subunit in the postfusion conformation, PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6B3O" id="ir0045">6B3O</ext-link>
. The prefusion to postfusion transition involves a “jack-knife” refolding of the HR1 helices and intervening regions into a single continuous helix appended to the central helix. The connector domain and HR2 in the prefusion structure and the fusion peptide in the postfusion structure of MHV were not resolved and are therefore not shown.</p>
</caption>
<alt-text id="al0020">Fig. 3</alt-text>
<graphic xlink:href="f04-03-9780128184561_lrg"></graphic>
</fig>
</p>
<p id="p0165">Recent structural work comparing recombinant S proteins from SARS-CoV and MERS-CoV in isolation and in complex with their cognate receptors or neutralizing antibodies suggested an activation mechanism for coronavirus fusion (<xref rid="bb0175" ref-type="bibr">Gui et al., 2017</xref>
; <xref rid="bb0230" ref-type="bibr">Kirchdoerfer et al., 2018</xref>
; <xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
; <xref rid="bb0470" ref-type="bibr">Song et al., 2018</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
; <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
). Specifically, SARS-CoV and MERS-CoV S structures in complex with neutralizing antibodies isolated from survivors showed both antibodies competitively blocked receptor interaction, in agreement with previous surface plasmon resonance data (<xref rid="bb0105" ref-type="bibr">Corti et al., 2015</xref>
; <xref rid="bb0420" ref-type="bibr">Rockx et al., 2008</xref>
; <xref rid="bb0510" ref-type="bibr">Traggiai et al., 2004</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
). The anti-SARS-CoV S230 antibody, however, functionally mimicked the receptor by promoting S fusogenic conformational rearrangements through a molecular ratcheting mechanism (<xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
) (<xref rid="f0025" ref-type="fig">Fig. 4</xref>
). These observations suggested that upon receptor recognition, bound B domains are locked in the open state, thereby releasing the constraints imposed on the HR1-central helix hairpin, allowing refolding of the S<sub>2</sub>
fusion machinery and membrane fusion to occur (<xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
; <xref rid="bb0470" ref-type="bibr">Song et al., 2018</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
; <xref rid="bb0660" ref-type="bibr">Yuan et al., 2017</xref>
) (<xref rid="f0025" ref-type="fig">Fig. 4</xref>
). Proteolytic activation is likely required to ensure that S glycoproteins will work in synergy, with proper spatial and temporal coordination, to drive fusion of the viral and host membranes.<fig id="f0025"><label>Fig. 4</label>
<caption><p>CryoEM structures of the SARS-CoV S glycoprotein in complex with the S230 neutralizing antibody. (A–B), Molecular surface representation of a complex with one open, one partially open, and one closed B domain, PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6NB6" id="ir0050">6NB6</ext-link>
(left) and with three open B domains that do not follow threefold symmetry, PDB: <ext-link ext-link-type="uri" xlink:href="pdb:6NB7" id="ir0055">6NB7</ext-link>
(right). The structures are rendered with different colors for each S protomer (light blue, plum and gold) and the S230 Fab heavy (dark magenta) and light (magenta) chains (only the variable domains are shown).</p>
</caption>
<alt-text id="al0025">Fig. 4</alt-text>
<graphic xlink:href="f04-04-9780128184561_lrg"></graphic>
</fig>
</p>
</sec>
<sec id="s0035"><label>6</label>
<title>Epitope masking and glycan shielding</title>
<p id="p0170">A deep knowledge of the organization and chemical composition of carbohydrates obstructing the surface of CoV S glycoproteins is key for understanding accessibility to neutralizing antibodies and for guiding the rational development of subunit vaccines and therapeutics. S glycoproteins feature ~ 20–35 predicted N-linked oligosaccharides per protomer. A cryoEM structure of the HCoV-NL63 S ectodomain allowed to visualize for the first time the extensive N-linked glycans covering the surface of a CoV S trimer (<xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
) (<xref rid="f0030" ref-type="fig">Fig. 5</xref>
). A subsequent study revealed that numerous glycosylation sites are strictly or topologically conserved between PDCoV S and HCoV-NL63 S although the two glycoproteins share only 43% amino acid sequence identity and the two viruses belong to different genera infecting different hosts (<xref rid="bb0600" ref-type="bibr">Xiong et al., 2018</xref>
). This observation suggested that all CoVs face similar immune pressure in their respective hosts, and that the areas that are masked by the conserved glycans might be key to the function of S. Based on the information gained from the HCoV-NL63 S structure, in which a glycan participates to masking the receptor-binding loops, it was proposed that the S glycan shield is involved in immune evasion, similarly to the well-characterized HIV-1 envelope trimer (<xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
).<fig id="f0030"><label>Fig. 5</label>
<caption><p>Organization of the HCoV-NL63 S glycan shield. Ribbon representation of the S ectodomain trimer with N-linked glycans rendered as dark-blue spheres, PDB: <ext-link ext-link-type="uri" xlink:href="pdb:5SZS" id="ir0060">5SZS</ext-link>
.</p>
</caption>
<alt-text id="al0030">Fig. 5</alt-text>
<graphic xlink:href="f04-05-9780128184561_lrg"></graphic>
</fig>
</p>
<p id="p0175">Comparison of the N-linked oligosaccharides of full-length MERS-CoV S derived from virions produced in African green monkey VeroE6 cells, or of a purified MERS-CoV S ectodomain recombinantly produced in HEK293F cells, revealed an extensive overlap of glycan composition, including the presence of hybrid and complex glycans (<xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
). Processed oligosaccharides were also observed decorating S trimers at the surface of authentic SARS-CoV virions (<xref rid="bb0250" ref-type="bibr">Krokhin et al., 2003</xref>
; <xref rid="bb0415" ref-type="bibr">Ritchie et al., 2010</xref>
). These data indicated that at least a fraction of the MERS-CoV and SARS-CoV virions produced in a cell are exposed to the glycan-processing enzymes residing in the Golgi apparatus during assembly and budding, in contrast with previous models of CoV budding (<xref rid="bb0350" ref-type="bibr">Ng et al., 2003</xref>
; <xref rid="bb0475" ref-type="bibr">Stertz et al., 2007</xref>
).</p>
<p id="p0180">A common feature observed in the glycosylation patterns of S glycoproteins is the presence of less densely glycosylated regions surrounding the S<sub>1</sub>
/S<sub>2</sub>
cleavage site and the conserved fusion peptide, near the S<sub>2</sub>
<sup>’</sup>
cleavage site, probably to allow access to activating host proteases and for membrane fusion to take place (<xref rid="bb0535" ref-type="bibr">Walls et al., 2016b</xref>
; <xref rid="bb0545" ref-type="bibr">Walls et al., 2019</xref>
) (<xref rid="f0030" ref-type="fig">Fig. 5</xref>
). These “glycan holes” could be targeted for epitope-focused immunogen design or new therapeutic development against CoV, as supported by the identification of a neutralization epitope within a comparable breach of the HIV-1 envelope glycan shield (<xref rid="bb0310" ref-type="bibr">McCoy et al., 2016</xref>
).</p>
</sec>
<sec id="s0040"><label>7</label>
<title>Concluding remarks</title>
<p id="p0185">Recent structural and functional characterization of CoV S glycoproteins provided insights into the mechanism used by these viruses to infect host cells and suggested possible strategies for rational design of vaccines and therapeutics. Introducing stabilizing mutations, which prevent the prefusion to postfusion S transition, led to the elicitation of improved neutralization titers in mice and will be a key tool for the design of subunit vaccines against CoVs (<xref rid="bb0230" ref-type="bibr">Kirchdoerfer et al., 2018</xref>
; <xref rid="bb0365" ref-type="bibr">Pallesen et al., 2017</xref>
). Furthermore, the exposure of the fusion peptide at the surface of prefusion S trimers (<xref rid="bb0530" ref-type="bibr">Walls et al., 2016a</xref>
) and its conservation among CoVs indicate it might be an attractive target for broad inhibition of CoV entry. Major antigenic determinants of MHV and SARS-CoV S overlap with the fusion peptide region (<xref rid="bb0110" ref-type="bibr">Daniel et al., 1993</xref>
; <xref rid="bb0665" ref-type="bibr">Zhang et al., 2004</xref>
) and binding of neutralizing antibodies to this site could putatively prevent fusogenic conformational changes, as proposed for influenza virus hemagglutinin or HIV envelope (<xref rid="bb0100" ref-type="bibr">Corti et al., 2011</xref>
; <xref rid="bb0235" ref-type="bibr">Kong et al., 2016</xref>
; <xref rid="bb0255" ref-type="bibr">Lang et al., 2017</xref>
). Finally, masking strain-specific antigenic regions <italic>via</italic>
engineering of additional N-linked glycosylation sites, as implemented for the MERS-CoV domain B (<xref rid="bb0130" ref-type="bibr">Du et al., 2016</xref>
), bears the promise of focusing the immune response on highly conserved epitopes and eliciting broadly neutralizing antibodies against CoVs.</p>
</sec>
</body>
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<ack id="ac0010"><title>Acknowledgments</title>
<p>We acknowledge support from the National Institute of General Medical Sciences (R01GM120553, D.V.), the National Institute of Allergy and Infectious Diseases (HHSN272201700059C, DV), a Pew Biomedical Scholars Award (D.V.), an Investigators in the Pathogenesis of Infectious Disease Award from the Burroughs Wellcome Fund (D.V.) and the Pasteur Institute (M.A.T.).</p>
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